Doxorubicin-induced oxidative stress in rats is efficiently counteracted by dietary anthocyanin differently enriched strawberry (Fragaria × ananassa Duch.)

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 18, 2014, Pages 3935-3943

  Diamanti, Jacopo ^a   Mezzetti, Bruno ^a   Giampieri, Francesca ^a   Alvarez Suarez, José M ^a   Quiles, José L ^b   Gonzalez Alonso, Adrian ^b   Ramirez Tortosa, Maria Del Carmen ^b   Granados Principal, Sergio ^b   Gonzáles Paramás, Ana M ^c   Santos Buelga, Celestino ^c   Battino, Maurizio ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF GRANADA   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

anthocyanins; DNA damage; doxorubicin; mitochondrial functionality; oxidative stress; strawberry

Indexed keywords

ANTHOCYANINS; ANTIOXIDANTS; DIETARY SUPPLEMENTS; DNA; NUTRITION; OXIDATIVE STRESS; RATS; TOXICITY; ENZYMES; FRUITS;

ANTIOXIDANT ENZYME ACTIVITY; DNA DAMAGES; DOXORUBICIN; MITOCHONDRIAL FUNCTIONALITY; OXIDATIVE STRESS BIOMARKERS; STRAWBERRY; STRAWBERRY CULTIVARS; TOTAL ANTIOXIDANT CAPACITY;

FRUITS; DIETARY SUPPLEMENTS;

FRAGARIA X ANANASSA; RATTUS;

ANTHOCYANIN; DOXORUBICIN;

ANIMAL; DIET THERAPY; DNA DAMAGE; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; ENZYMOLOGY; FRAGARIA; GENETICS; HUMAN; LIVER; MALE; METABOLISM; MITOCHONDRION; OXIDATIVE STRESS; RAT; WISTAR RAT;

ANIMALS; ANTHOCYANINS; DNA DAMAGE; DOXORUBICIN; DRUG-INDUCED LIVER INJURY; FRAGARIA; HUMANS; LIVER; MALE; MITOCHONDRIA; OXIDATIVE STRESS; RATS; RATS, WISTAR;

EID: 84900300051     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf405721d     Document Type: Article

References (50)

1. Granados-Principal, S.; Quiles, J. L.; Ramirez-Tortosa, C. L.; Sanchez-Rovira, P.; Ramirez-Tortosa, M. C. New advances in molecular mechanisms and the prevention of adriamycin toxicity by antioxidant nutrients Food Chem. Toxicol. 2010, 48, 1425-1438
2. Nettleton, J. A.; Steffen, L. M.; Mayer-Davis, E. J. Dietary patterns are associated with biochemical markers of inflammation and endothelial activation in the multi-ethnic study of atherosclerosis (MESA) Am. J. Clin. Nutr. 2006, 83, 1369-1379
3. Helmersson, J.; Arnlov, J.; Larsson, A.; Basu, S. Low dietary intake of β-carotene, α-tocopherol and ascorbic acid is associated with increased inflammatory and oxidative stress status in a Swedish cohort Br. J. Nutr. 2009, 101, 1775-1782
4. Bach-Faig, A.; Berry, E. M.; Lairon, D.; Reguant, J.; Trichopoulou, A.; Dernini, S.; Medina, F. X.; Battino, M.; Belahsen, R.; Miranda, G.; Serra-Majem, L. Mediterranean diet foundation expert group. Mediterranean diet pyramid today. Science and cultural updates Public Health Nutr. 2011, 14, 2274-2284
5. Giampieri, F.; Tulipani, S.; Alvarez-Suarez, J. M.; Quiles, J. L.; Mezzetti, B.; Battino, M. The strawberry: composition, nutritional quality, and impact on human health Nutrition 2012, 28, 9-19
6. Giampieri, F.; Alvarez-Suarez, J. M.; Mazzoni, L.; Romandini, S.; Bompadre, S.; Diamanti, J.; Capocasa, F.; Mezzetti, B.; Quiles, J. L.; Ferreiro, M. S.; Tulipani, S.; Battino, M. The potential impact of strawberry on human health Nat. Prod. Res. 2013, 27, 448-455
7. Seeram, N. P.; Heber, D. Impact of berry phytochemicals on human health: effects beyond antioxidation. In Antioxidant Measurement and Applications; ACS Symposium Series 956; American Chemical Society: Washington, DC, USA, 2006; Chapter 21, pp 326-336.
8. Boivin, D.; Blanchette, M.; Barrette, S.; Moghrabi, A.; Beliveau, R. Inhibition of cancer cell proliferation and suppression of TNF induced activation of NFκB by edible berry juice Anticancer Res. 2007, 27, 937-948
9. Starvic, B.; Matula, T. I.; Klassen, R.; Downie, R. H.; Wood, R. J. Effect of flavonoids on mutagenicity and bioavailability of xenobiotics in food.. In Phenolic Compounds in Food and Their Effects on Health II. Antioxidants & Cancer Prevention; ACS Symposium Series 507; American Chemical Society: Washington, DC, USA, 1992; Chapter 17, pp 239-249.
10. Diamanti, J.; Capocasa, F.; Battino, M.; Mezzetti, B. Evaluation of F. × ananassa intra-specific and inter-specific back-crosses to generate new genetic material with increased fruit nutritional quality J. Berry Res. 2010, 1, 103-114
11. Diamanti, J.; Capocasa, F.; Balducci, F.; Battino, M.; Hancock, J.; Mezzetti, B. Increasing strawberry fruit sensorial and nutritional quality using wild and cultivated germplasm PLoS One 2012, 7, e46470
12. Diamanti, J.; Capocasa, F.; Denoyes, B.; Petit, A.; Chartier, P.; Faedi, W.; Maltoni, M. L.; Battino, M.; Mezzetti, B. Standardized method for evaluation of strawberry (Fragaria × ananassa Duch.) germplasm collections as a genetic resource for fruit nutritional compounds J. Food Compos. Anal. 2012, 28, 170-178
13. Tulipani, S.; Mezzetti, B.; Capocasa, F.; Bompadre, S.; Beekwilder, J.; de Vos, C. H.; Capanoglu, E.; Bovy, A.; Battino, M. Antioxidants, phenolic compounds, and nutritional quality of different strawberry genotypes J. Agric. Food Chem. 2008, 56, 696-704
14. Lopes da Silva, F.; Escribano-Bailon, M. T.; Perez-Alonso, J. J.; Rivas-Gonzalo, J.; Santos-Buelga, C. Anthocyanin pigments in strawberry LWT-Food Sci. Technol. 2007, 40, 374-382
15. Prior, R. L.; Wu, X.; Gu, L.; Hager, T. J.; Hager, A.; Howard, L. R. Whole berries versus berry anthocyanins: interactions with dietary fat levels in the C57BL/6J mouse model of obesity J. Agric. Food Chem. 2008, 56, 647-653
16. Quiles, J. L.; Ramirez-Tortosa, M. C.; Huertas, J. R.; Ibañez, S.; Gomez, J. A.; Battino, M.; Mataix, J. Olive oil supplemented with vitamin E affects mitochondrial coenzyme Q levels in liver of rats after an oxidative stress induced by adriamycin Biofactors 1999, 9, 331-336
17. Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the Folin phenol reagent J. Biol. Chem. 1951, 193, 265-275
18. Quiles, J. L.; Ochoa, J. J.; Battino, M.; Gutierrez-Rios, P.; Nepomuceno, E. A.; Frías, M. L.; Huertas, J. R.; Mataix, J. Life-long supplementation with a low dosage of coenzyme Q10 in the rat: effects on antioxidant status and DNA damage Biofactors 2005, 25, 73-86
19. Levine, R. L.; Garland, D.; Oliver, C. N.; Amici, A.; Climent, I.; Lenz, A. G.; Ahn, B. W.; Shaltiel, S.; Stadtman, E. R. Determination of carbonyl content in oxidatively modified proteins Methods Enzymol. 1990, 186, 464-478
20. Ellman, G. L. Tissue sulfahydryl groups Arch. Biochem. Biophys. 1959, 82, 70-77
21. Ohkawa, H.; Ohishi, N.; Yagi, K. Assay for lipid peroxide in animal tissue by thiobarbituric acid reaction Anal. Biochem. 1979, 95, 331-358
22. Jiang, Z. Y.; Hunt, J. V.; Wolff, S. P. Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein Anal. Biochem. 1992, 202, 384-389
23. Aebi, H. Catalase in vitro Methods Enzymol. 1984, 105, 121-126
24. Kakkar, P.; Das, B.; Viswanathan, P. N. A modified spectrophotometric assay of superoxide dismutase Indian J. Biochem. Biophys. 1984, 21, 130-132
25. Sies, H.; Koch, O. R.; Martino, E.; Boveris, A. Increased biliary glutathione disulfide release in chronically ethanol treated rats FEBS Lett. 1979, 103, 287-290
26. Carlberg, I.; Mannervik, B. Glutathione reductase Methods Enzymol. 1985, 113, 484-490
27. Habig, W. H.; Pabst, M. J.; Jacoby, W. B. Glutathione-S-transferase: the first enzymatic step in mercapturic acid formation J. Biol. Chem. 1974, 249, 7130-7139
28. Rogers, G. W.; Brand, M. D.; Petrosyan, S.; Ashok, D.; Elorza, A. A.; Ferrick, D. A.; Murphy, A. N. High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria PLoS One 2011, 6, e21746
29. Buendía, B.; Gil, M. I.; Tudela, J. A.; Gady, A. L.; Medina, J. J.; Soria, C.; López, J. M.; Tomás-Barberán, F. A. HPLC-MS analysis of proanthocyanidin oligomers and other phenolics in 15 strawberry cultivars J. Agric. Food Chem. 2010, 58, 3916-3926
30. Vrhovsek, U.; Guella, G.; Gasperotti, M.; Pojer, E.; Zancato, M.; Mattivi, F. Clarifying the identity of the main ellagitannin in the fruit of the strawberry, Fragaria vesca and Fragaria ananassa Duch J. Agric. Food Chem. 2012, 60, 2507-2516
31. Nieminen, A. L.; Byrne, A. M.; Herman, B.; Leemasters, J. J. Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species Am. J. Physiol. 1997, 272, 1286-1294
32. Stoner, G. D.; Chen, T.; Kresty, L. A.; Aziz, R. M.; Reinemann, T.; Nines, R. Protection against esophageal cancer in rodents with lyophilized berries: potential mechanisms Nutr. Cancer 2006, 54, 33-46
33. Quiles, J. L.; Ochoa, J. J.; Ramirez-Tortosa, C.; Battino, M.; Huertas, J. R.; Martín, Y.; Mataix, J. Dietary fat type (virgin olive vs. sunflower oils) affects age-related changes in DNA double-strand-breaks, antioxidant capacity and blood lipids in rats Exp. Gerontol. 2004, 39, 1189-1198
34. Gülkaç, M. D.; Akpinar, G.; Ustün, H.; Ozön Kanli, A. Effects of vitamin A on doxorubicin-induced chromosomal aberrations in bone marrow cells of rats Mutagenesis 2004, 19, 231-236
35. Kalender, Y.; Yel, M.; Kalender, S. Doxorubicin hepatotoxicity and hepatic free radical metabolism in rats. The effects of vitamin E and catechin Toxicology 2005, 209, 39-45
36. Liu, W.; Lu, X.; He, G.; Gao, X.; Li, M.; Wu, J.; Li, Z.; Wang, J.; Luo, C. Cytosolic protection against ultraviolet induced DNA damage by blueberry anthocyanins and anthocyanidins in hepatocarcinoma HepG2 cells Biotechnol. Lett. 2013, 35, 491-498
37. Giampieri, F.; Alvarez-Suarez, J. M.; Tulipani, S.; Gonzàles- Paramàs, A. M.; Santos-Buelga, C.; Bompadre, S.; Quiles, J. L.; Mezzetti, B.; Battino, M. Photoprotective potential of strawberry (Fragaria × ananassa) extract against UV-A irradiation damage on human fibroblasts J. Agric. Food Chem. 2012, 60, 2322-2327
38. Cimino, F.; Ambra, R.; Canali, R.; Saija, A.; Virgili, F. Effect of cyanidin-3- O -glucoside on UVB-induced response in human keratinocytes J. Agric. Food Chem. 2006, 54, 4041-4047
39. Duthie, S. J.; Jenkinson, A. M.; Crozier, A.; Mullen, W.; Pirie, L.; Kyle, J.; Yap, L. S.; Christen, P.; Duthie, G. G. The effects of cranberry juice consumption on antioxidant status and biomarkers relating to heart disease and cancer in healthy human volunteers Eur. J. Nutr. 2006, 45, 113-122
40. Moller, P.; Loft, S.; Alfthan, G.; Freese, R. Oxidative DNA damage in circulating mononuclear blood cells after ingestion of blackcurrant juice or anthocyanin-rich drink Mutat. Res. 2004, 551, 119-126
41. Wilms, L. C.; Hollman, P. C.; Boots, A. W.; Kleinjans, J. C. Protection by quercetin and quercetin-rich fruit juice against induction of oxidative DNA damage and formation of BPDE-DNA adducts in human lymphocytes Mutat. Res. 2005, 582, 155-162
42. Weisel, T.; Baum, M.; Eisenbrand, G.; Dietrich, H.; Will, F.; Stockis, J. P.; Kulling, S.; Rüfer, C.; Johannes, C.; Janzowski, C. An anthocyanin/polyphenolic-rich fruit juice reduces oxidative DNA damage and increases glutathione level in healthy probands Biotechnol. J. 2006, 1, 388-397
43. Wilms, L. C.; Boots, A. W.; de Boer, V. C.; Maas, L. M.; Pachen, D. M.; Gottschalk, R. W.; Ketelslegers, H. B.; Godschalk, R. W.; Haenen, G. R.; van Schooten, F. J.; Kleinjans, J. C. Impact of multiple genetic polymorphisms on effects of a 4-week blueberry juice intervention on ex vivo induced lymphocytic DNA damage in human volunteers Carcinogenesis 2007, 28, 1800-1806
44. Traustadóttir, T.; Davies, S. S.; Stock, A. A.; Su, Y.; Heward, C. B.; Roberts, L. J.; Harman, S. M. Tart cherry juice decreases oxidative stress in healthy older men and women J. Nutr. 2009, 139, 1896-1900
45. Ramirez-Tortosa, C.; Andersen, O. M.; Gardner, P. T.; Morrice, P. C.; Wood, S. G.; Duthie, S. J.; Collins, A. R.; Duthie, G. C. Anthocyanin rich extract decreases indices of lipid peroxidation and DNA damage in vitamin E-depleted rats Free Radical Biol. Med. 2001, 31, 1033-1037
46. Shih, P. H.; Yeh, C. T.; Yen, G. C. Anthocyanins induce the activation of phase II enzymes through the antioxidant response element pathway against oxidative stress-induced apoptosis J. Agric. Food Chem. 2007, 55, 9427-9435
47. Boateng, J.; Verghese, M.; Shackelford, L.; Walker, L. T.; Khatiwada, J.; Ogutu, S.; Williams, D. S.; Jones, J.; Guyton, M.; Asiamah, D.; Henderson, F.; Grant, L.; DeBruce, M.; Johnson, A.; Washington, S.; Chawan, C. B. Selected fruits reduce azoxymethane (AOM)-induced aberrant crypt foci (ACF) in Fisher 344 male rats Food Chem. Toxicol. 2007, 45, 725-732
48. Alvarez-Suarez, J. M.; Dekanski, D.; Ristić, S.; Radonjić, N. V.; Petronijević, N. D.; Giampieri, F.; Astolfi, P.; González-Paramás, A. M.; Santos-Buelga, C.; Tulipani, S.; Quiles, J. L.; Mezzetti, B.; Battino, M. Strawberry polyphenols attenuate ethanol-induced gastric lesions in rats by activation of antioxidant enzymes and attenuation of MDA increase PLoS One 2011, 6 (10) e25878
49. Fiorani, M.; Guidarelli, A.; Blasa, M.; Azzolini, C.; Candiracci, M.; Piatti, E.; Cantoni, O. Mitochondria accumulate large amounts of quercetin: prevention of mitochondrial damage and release upon oxidation of the extramitochondrial fraction of the flavonoid J. Nutr. Biochem. 2010, 21, 397-404
50. Steele, V. E.; Kelloff, G. J.; Balentine, D.; Boone, C. W.; Mehta, R.; Bagheri, D.; Sigman, C. C.; Zhu, S.; Sharma, S. Comparative chemopreventive mechanisms of green tea, black tea and selected polyphenol extracts measured by in vitro bioassays Carcinogenesis 2000, 21, 63-67